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Normalization of cell responses in cat striate cortex

Published online by Cambridge University Press: 02 June 2009

David J. Heeger
Affiliation:
NASA-Ames Research Center, Moffett Field, California and Department of Psychology, Stanford University, Stanford, California

Abstract

Simple cells in the striate cortex have been depicted as half-wave-rectified linear operators. Complex cells have been depicted as energy mechanisms, constructed from the squared sum of the outputs of quadrature pairs of linear operators. However, the linear/energy model falls short of a complete explanation of striate cell responses. In this paper, a modified version of the linear/energy model is presented in which striate cells mutually inhibit one another, effectively normalizing their responses with respect to stimulus contrast. This paper reviews experimental measurements of striate cell responses, and shows that the new model explains a significantly larger body of physiological data.

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Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Adelson,E.H. &Bergen,J.R. (1985).Spatiotemporal energy models for the perception of motion.Journal of the Optical Society of America A2,284–299.CrossRefGoogle ScholarPubMed
Albrecht,D.G.,Farrar,S.B. &Hamilton,D.B. (1984).Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex.Journal of Physiology (London)347,713–739.CrossRefGoogle ScholarPubMed
Albrecht,D.G. &Geisler,W.S. (1991).Motion sensitivity and the contrast-response function of simple cells in the visual cortex.Visual Neuroscience7,531–546.CrossRefGoogle ScholarPubMed
Albrecht,D.G. &Hamilton,D.B. (1982).Striate cortex of monkey and cat: Contrast response function.Journal of Neurophysiology48,217–237.CrossRefGoogle ScholarPubMed
Bishop,P.O.,Coombs,J.S. &Henry,G.H. (1973).Receptive fields of simple cells in the cat striate cortex.Journal of Physiology (London)231,31–60.CrossRefGoogle ScholarPubMed
Blakemore,C. &Tobin,E.A. (1972).Lateral inhibition between orientation detectors in the cat's visual cortex.Experimental Brain Research15,439–440.CrossRefGoogle ScholarPubMed
Bolz,J. &Gilbert,C.D. (1986).Generation of end-inhibition in the visual cortexvia interlaminar connections.Nature320,362–365.CrossRefGoogle ScholarPubMed
Bonds,A.B. (1989).Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex.Visual Neuroscience2,41–55.CrossRefGoogle ScholarPubMed
Bonds,A.B. (1991).Temporal dynamics of contrast gain in single cells of the cat striate cortex.Visual Neuroscience6,239–255.CrossRefGoogle ScholarPubMed
Bonds,A.B.,DeBusk,B.C. &Ming,S. (1990).Stimulation far beyond the receptive field of cat striate cortical cells strongly mediates responsiveness: A mechanism for global inhibition.Investigative Opthalmology and Visual Science (Suppl.)31,429.Google Scholar
Bullier,J. &Henry,G.H. (1979a).Ordinal position of neurons in cat striate cortex.Journal of Neurophysiology42,1251–1263.CrossRefGoogle ScholarPubMed
Bullier,J. &Henry,G.H. (1979b).Neural path taken by afferent streams in striate cortex of the cat.Journal of Neurophysiology42,1264–1270.CrossRefGoogle ScholarPubMed
Bullier,J. &Henry,G.H. (1979c).Laminar distribution of first-order neurons and afferent terminals in cat striate cortex.Journal of Neurophysiology42,1271–1281.CrossRefGoogle ScholarPubMed
Campbell,F.W.,Cooper,G.F. &Enroth-Cugell,C. (1968).The angular selectivity of visual cortical cells to moving gratings.Journal of Physiology (London)198,237–250.CrossRefGoogle ScholarPubMed
Campbell,F.W.,Cooper,G.F. &Enroth-Cugell,C. (1969).The spatial selectivity of visual cells of the cat.Journal of Phvsiology (London)203,223–235.Google ScholarPubMed
Chao-Yi,Li. &Creutzfeldt,O. (1984).The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat.Pflugers Archives401,304–314.CrossRefGoogle Scholar
Dean,A.F. (1980).The contrast-dependence of direction selectivity.Journal of Physiology (London)303,38p-39p.Google Scholar
Dean,A.F. (1981).The relationship between response amplitude and contrast for cat striate cortical neurones.Journal of Physiology (London)318,413–427.CrossRefGoogle ScholarPubMed
Dean,A.F. (1983).Adaptation-induced alteration of the relation between response amplitude and contrast in cat striate cortical mechanisms.Vision Research23,249–256.CrossRefGoogle Scholar
Dean,A.F.,Hess,R.F. &Tolhurst,D.J. (1980).Divisive inhibition involved in direction selectivity.Journal of Physiology (London)308,84p-85p.Google Scholar
Dean,A.F. &Tolhurst,D.J. (1983).On the distinctiveness of simple and complex cells in the visual cortex of the cat.Journal of Physiology (London)344,305–325.CrossRefGoogle ScholarPubMed
Dean,A.F. &Tolhurst,D.J. (1986).Factors influencing the temporal phase of response to bar and grating stimuli for simple cells in the cat striate cortex.Experimental Brain Research62,143–151.CrossRefGoogle ScholarPubMed
Dean,A.F.,Tolhurst,D.J. &Walker,N.S. (1982).Nonlinear temporal summation by simple cells in cat striate cortex demonstrated by failure of superposition.Experimental Brain Research45,456–458.CrossRefGoogle ScholarPubMed
DeAngelis,G.C.,Ohzawa,I.,Freeman,R.D. &Ghose,G. (1990).Properties of length and width tuning of cells in the cat's striate cortex.Investigative Opthalmology and Visual Science (Suppl.)32,430.Google Scholar
DeAngelis,G.C.,Robson,J.G.,Ohzawa,I. &Freeman,R.D. (1992). The organization of suppression in receptive fields of neurons in the cat's visual cortex.Journal of Neurophysiology (in press).Google Scholar
DeBruvn,E.J. &Bonds,A.B. (1986).Contrast adaptation in the cat is not mediated by GABA.Brain Research383,339–342.CrossRefGoogle Scholar
Derrington,A.M. &Lennie,P. (1984).Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque.Journal of Physiology (London)357,219–240.CrossRefGoogle ScholarPubMed
DeValois,K. &Tootell,R. (1983).Spatial-frequency-specific inhibition in cat striate cortex cells.Journal of Physiology (London)336,359–376.CrossRefGoogle Scholar
DeValois,R.L.,Thorell,L.G. &Albrecht,D.G. (1985).Periodicity of striate-cortex-cell receptive fields.Journal of the Optical Society of America A2,1115–1123.CrossRefGoogle Scholar
Douglas,R.J.,Martin,K.A.C. &Whitteridge,D. (1988).Selective responses of visual cortical cells do not depend on shunting inhibition.Nature332,642–644.CrossRefGoogle Scholar
Dreher,B. (1972).Hypercomplex cells in the cat's striate cortex.Investigative Opthalmology11,355–356.Google ScholarPubMed
Emerson,R.C. &Citron,M.C. (1989). Linear and nonlinear mechanisms of motion selectivity in single neurons of the cat's visual cortex. InProceedings of IEEE International Conference on Systems, Man, and Cybernetics, ed pp.448–453.Cambridge, Massachusetts:IEEE.CrossRefGoogle Scholar
Ferster,D. (1981).A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex.Journal of Physiology (London)311,623–655.CrossRefGoogle ScholarPubMed
Ferster,D. &Lindstrom,S. (1983).An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat.Journal of Physiology (London)342,181–215.CrossRefGoogle ScholarPubMed
Freeman,R.D.,Ohzawa,I. &Robson,J.G. (1987).A comparison of monocular and binocular inhibitory processes in the visual cortex of cat.Journal of Physiology (London)396,69p.Google Scholar
Gilbert,C.D. (1977).Laminar differences in receptive properties of cells in cat primary visual cortex.Journal of Physiology (London)268,391–421.CrossRefGoogle ScholarPubMed
Gilbert,C.D. &Wiesel,T.N. (1990).The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat.Vision Research30,1689–1701.CrossRefGoogle ScholarPubMed
Glezer,V.D.,Tscherbach,T.A.,Gauselman,V.E. &Bondarko,V.E. (1980).Linear and nonlinear properties of simple and complex receptive fields in area 17 of the cat visual cortex.Biological Cybernetics37,195–208.CrossRefGoogle ScholarPubMed
Glezer,V.D.,Tscherbach,T.A.,Gauselman,V.E. &Bondarko,V.E. (1982).Spatio-temporal organization of receptive fields of the cat striate cortex.Biological Cybernetics43,35–49.CrossRefGoogle ScholarPubMed
Gulyas,B.,Orban,G.A.,Duysens,J. &Maes,H. (1987).The suppressive influence of moving textured backgrounds on responses of cat striate neurons to moving bars.Journal of Neurophysiology57,1767–1791.CrossRefGoogle ScholarPubMed
Hammond,P. &Ahmed,B. (1985).Length summation of complex cells in cat striate cortex: A reappraisal of the special/standard classification.Neuroscience15,639–649.CrossRefGoogle ScholarPubMed
Hammond,P. &MacKay,D.M. (1977).Differential responsiveness of simple and complex cells in cat striate cortex to visual texture.Experimental Brain Research30,275–296.Google ScholarPubMed
Hammond,P. &MacKay,D.M. (1978).Modulation of simple cell activity in cat by moving textured backgrounds.Journal of Physiology (London)284,117p.Google ScholarPubMed
Hammond,P. &MacKay,D.M. (1981).Modulatory influences of moving textured backgrounds on responsiveness of simple cells in feline striate cortex.Journal of Physiology (London)319,431–442.CrossRefGoogle ScholarPubMed
Hammond,P.,Mouat,G.S. &Smith,A.T. (1985).Motion after-effects in cat striate cortex elicited by moving gratings.Experimental Brain Research60,411–416.CrossRefGoogle ScholarPubMed
Hammond,P.,Mouat,G.S. &Smith,A.T. (1986).Motion after-effects in cat striate cortex elicited by moving texture.Vision Research26,1055–1060.CrossRefGoogle ScholarPubMed
Hammond,P.,Mouat,G.S. &Smith,A.T. (1988).Neural correlates of motion after-effects in cat striate cortical neurones: Monocular adaptation.Experimental Brain Research72,1–20.CrossRefGoogle ScholarPubMed
Hammond,P.,Pomfrett,C.J.D. &Ahmed,B. (1989).Neural motion after-effects in the cat's striate cortex: Orientation selectivity.Vision Research29,1671–1683.CrossRefGoogle ScholarPubMed
Hata,Y.,Tsumoto,T.,Sato,H.,Hagihara,K. &Tamura,H. (1988).Inhibition contributes to orientation selectivity in visual cortex of cat.Nature335,815–817.CrossRefGoogle ScholarPubMed
Heeger,D.J. (1990).Nonlinear model of cat striate physiology.Society for Neuroscience Abstracts16,229.Google Scholar
Heeger,D.J. (1991). Nonlinear model of neural responses in cat visual cortex. InComputational Models of Visual Processing, edLandy,M.,Movshon,J.A., pp.119–133.Cambridge, Massachusetts:MIT Press.Google Scholar
Heeger,D.J. (1992a). Half-squaring in responses of cat simple cells.Visual Neuroscience (in press).Google Scholar
Heeger,D.J. (1992b).Modeling simple cell direction selectivity with normalized, half-squared, linear operators.Investigative Ophthalmology and Visual Science (Suppl.)33 (in press).Google Scholar
Heeger,D.J. &Adelson,E.H. (1989).Nonlinear model of cat striate cortex.Optics News15, A-42.Google Scholar
Hess,R.,Negishi,K. &Creutzfeldt,O.D. (1975).The horizontal spread of intracortical inhibition in the visual cortex.Experimental Brain Research22,415–419.CrossRefGoogle Scholar
Hoffman,K.R. &Stone,J. (1971).Conduction velocity of afferent to cat visual cortex: A correlation with cortical receptive fields of single cells in cat striate cortex.Brain Research32,460–466.CrossRefGoogle Scholar
Holub,R.A. &Morton-Gibson,M. (1981).Response of visual cortical neurons of the cat to moving sinusoidal gratings: Response-contrast functions and spatiotemporal integration.Journal of Neurophysiology46,1244–1259.CrossRefGoogle Scholar
Hubel,D. &Wiesel,T. (1962).Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex.Journal of Physiology (London)160,106–154.CrossRefGoogle ScholarPubMed
Hubel,D. &Wiesel,T. (1965).Receptive field and functional architecture in two nonstriate visual areas (18–19) of the cat.Journal of Neurophysiology28,229–289.CrossRefGoogle Scholar
Kaji,S. &Kawabata,N. (1985).Neural interactions of two moving patterns in the direction and orientation domain in the complex cells of cat's visual cortex.Vision Research25,749–753.CrossRefGoogle ScholarPubMed
Kato,H.,Bishop,P.O. &Orban,G.A. (1978).Hypercomplex and simple/complex cell classifications in cat striate cortex.Journal of Neurophysiology41,1071–1095.CrossRefGoogle ScholarPubMed
Kulikowski,J.J. &Bishop,P.O. (1982).Silent periodic cells in the cat striate cortex.Vision Research22,191–200.CrossRefGoogle ScholarPubMed
Kulikowski,J.J.,Bishop,P.O. &Kato,H. (1981).Spatial arrangement of responses by cells in the cat visual cortex to light and dark bars and edges.Experimental Brain Research44,371–385.CrossRefGoogle ScholarPubMed
Maddess,T.,McCourt,M.E.,Blakeslee,B. &Cunningham,R.B. (1988).Factors governing the adaptation of cells in area 17 of the cat visual cortex.Biological Cybernetics59,229–236.CrossRefGoogle ScholarPubMed
Maffei,L. &Fiorentini,A. (1973).The visual cortex as a spatialfrequency analyzer.Vision Research13,1255–1267.CrossRefGoogle Scholar
Maffei,L. &Fiorentini,A. (1976).The unresponsive regions of visual cortical receptive fields.Vision Research16,1131–1139.CrossRefGoogle ScholarPubMed
Maffei,L.,Fiorentini,A. &Bisti,S. (1973).Neural correlate of perceptual adaptation to gratings.Science182,1036–1038.CrossRefGoogle ScholarPubMed
Marlin,S.G.,Hasan,S.J. &Cynader,M.S. (1988).Direction-selective adaptation in simple and complex cells in cat striate cortex.Journal of Neurophysiology59,1314–1330.CrossRefGoogle ScholarPubMed
Martin,K.A.C. &Whitteridge,D. (1984).Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat.Journal of Physiology (London)353,463–504.CrossRefGoogle ScholarPubMed
McLean,J. &Palmer,L.A. (1989).Contribution of linear spatiotemporal receptive-field structure to velocity selectivity of simple cells in area 17 of cat.Vision Research29,675–679.CrossRefGoogle ScholarPubMed
Morrone,M.C.,Burr,D.C. &Maffei,L. (1982).Functional implications of cross-orientation inhibition of cortical visual cells.Proceedings of the Royal Society B (London)216,335–354.Google ScholarPubMed
Movshon,J.A. (1975).The velocity tuning of single units in cat striate cortex.Journal of Physiology (London)249,445–468.CrossRefGoogle ScholarPubMed
Movshon,J.A. &Lennie,P. (1979).Pattern-selective adaptation in visual cortical neurones.Nature278,850–852.CrossRefGoogle ScholarPubMed
Movshon,J.A.,Thompson,I.D. &Tolhurst,D.J. (1978a).Spatial summation in the receptive fields of simple cells in the cat's striate cortex.Journal of Physiology (London)283,53–77.CrossRefGoogle ScholarPubMed
Movshon,J.A.,Thompson,I.D. &Tolhurst,D.J. (1978b).Receptive-field organization of complex cells in the cat's striate cortex.Journal of Physiology (London)283,79–99.CrossRefGoogle ScholarPubMed
Movshon,J.A.,Thompson,I.D. &Tolhurst,D.J. (1978c).Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex.Journal of Physiology (London)283,101–120.CrossRefGoogle ScholarPubMed
Murphy,P.C. &Sillito,A.M. (1987).Corticofugal feedback influences the generation of length tuning in the visual pathway.Nature329,727–729.CrossRefGoogle ScholarPubMed
Nelson,J.I.,Lingner,I. &Bremmer,F. (1991).Adaptation and disadaptation in cat A17 cells stimulated only beyond their classic receptive fields.Investigative Ophthalmology and Visual Science (Suppl.)32,1252.Google Scholar
Nelson,J.J. &Frost,B.J. (1978).Orientation-selective inhibition from beyond the classic visual receptive field.Brain Research139,359–365.CrossRefGoogle ScholarPubMed
Nelson,S.B. (1991).Temporal interactions in the cat visual system. I. Orientation-selective suppression in visual cortex.Journal of Neuroscience11,344–356.CrossRefGoogle ScholarPubMed
Ohzawa,I. &Freeman,R.D. (1986).The binocular organization of simple cells in the cat's visual cortex.Journal of Neurophysiology56,221–242.CrossRefGoogle ScholarPubMed
Ohzawa,I.,Sclar,G. &Freeman,R.D. (1982).Contrast gain control in the cat visual cortex.Nature298,266–268.CrossRefGoogle ScholarPubMed
Ohzawa,I.,Sclar,G. &Freeman,R.D. (1985).Contrast gain control in the cat's visual system.Journal of Neurophysiology54,651–667.CrossRefGoogle ScholarPubMed
Pettigrew,J.D.,Nikara,T. &Bishop,P.O. (1968).Responses to moving slits by single units in cat striate cortex.Experimental Brain Research6,373–390.Google ScholarPubMed
Pollen,D. &Ronner,S. (1983).Visual cortical neurons as localized spatial-frequency filters.IEEE Transactions on Systems, Man, and Cybernetics13,907–916.CrossRefGoogle Scholar
Pollen,D.A.,Andrews,B.W. &Feldon,S.E. (1978).Spatial-frequency selectivity of periodic complex cells in the visual cortex of the cat.Vision Research18,665–682.CrossRefGoogle ScholarPubMed
Pollen,D.A.,Gaska,J.P. &Jacobson,L.D. (1989). Physiological constraints on models of visual cortical function.In Models of Brain Function, edCotterill,R.M.J.,Cambridge University Press.Google Scholar
Reid,R.C.,Soodak,R.E. &Shapley,R.M. (1987).Linear mechanisms of directional selectivity in simple cells of cat striate cortex.Proceedings of the National Academy of Sciences of the U.S.A.84,8740–8744.CrossRefGoogle ScholarPubMed
Reid,R.C.,Soodak,R.E. &Shapley,R.M. (1991).Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex.Journal of Neurophysiology66,505–529.CrossRefGoogle ScholarPubMed
Robson,J.G. (1988).Linear and nonlinear operations in the visual system.Investigative Ophthalmology and Visual Science (Suppl.)29,117.Google Scholar
Robson,J.G.,Deangelis,G.C.,Ohzawa,I. &Freeman,R.D. (1991).Cross-orientation inhibition in cat cortical cells originates from within the receptive field.Investigative Ophthalmology and Visual Science (Suppl.)32,429.Google Scholar
Rose,D. (1977).Responses of single units in cat visual cortex to moving bars of light as a function of bar length.Journal of Physiology (London)271,1–23.CrossRefGoogle ScholarPubMed
Saul,A.B. &Cynader,M.S. (1989a).Adaptation in single units in the visual cortex: The tuning of aftereffects in the spatial domain.Visual Neuroscience2,593–607.CrossRefGoogle ScholarPubMed
Saul,A.B. &Cynader,M.S. (1989b).Adaptation in single units in the visual cortex: The tuning of aftereffects in the temporal domain.Visual Neuroscience2,609–620.CrossRefGoogle ScholarPubMed
Sclar,G. &Freeman,R.D. (1982).Orientation selectivity of the cat's striate cortex is invariant with stimulus contrast.Experimental Brain Research46,457–461.CrossRefGoogle ScholarPubMed
Sclar,G.,Maunsell,J.H.R. &Lennie,P. (1990).Coding of image contrast in central visual pathways of the macaque monkey.Vision Research30,1–10.CrossRefGoogle ScholarPubMed
Shapley,R. &Enroth-Cugell,C. (1984).Visual adaptation and retinal gain control.Progress in Retinal Research3,263–346.CrossRefGoogle Scholar
Singer,W.,Tretter,F. &Cynader,M. (1975).Organization of cat striate cortex: A correlation of receptive-field properties with afferent and efferent connections.Journal of Neurophysiology38,1080–1098.CrossRefGoogle ScholarPubMed
Skottun,B.C.,Bradley,A.,Sclar,G.,Ohzawa,I. &Freeman,R.D. (1987).The effects of contrast on visual orientation and spatial-frequency discrimination: A comparison of single cells and behavior.Journal of Neurophysiology57,773–786.CrossRefGoogle ScholarPubMed
Spekreuse,H. &van den Berg,T.J.T.P. (1971).Interaction between colour and spatial coded processes converging to retinal ganglion cells in goldfish.Journal of Physiology (London)215,679–692.CrossRefGoogle Scholar
Sperling,G. &Sondhi,M.M. (1968).Model for visual luminance discrimination and flicker detection.Journal of the Optical Society of America58,1133–1145.CrossRefGoogle ScholarPubMed
Stone,J. &Dreher,B. (1973).Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex.Journal of Neurophysiology36,551–567.CrossRefGoogle ScholarPubMed
Tanaka,K. (1983).Cross-correlation analysis of geniculostriate neuronal relationships in cats.Journal of Neurophysiology49,1303–1318.CrossRefGoogle ScholarPubMed
Tanaka,K. (1985).Organization of geniculate inputs to visual cortical cells in the cat.Vision Research25,357–364.CrossRefGoogle ScholarPubMed
Tolhurst,D.J. &Dean,A.F. (1987).Spatial summation by simple cells in the striate cortex of the cat.Experimental Brain Research66,607–620.CrossRefGoogle ScholarPubMed
Tolhurst,D.J. &Dean,A.F. (1991).Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex.Visual Neuroscience6,421–428.CrossRefGoogle ScholarPubMed
Tolhurst,D.J.,Walker,N.S.,Thompson,I.D. &Dean,A.F. (1980).Nonlinearities of temporal summation in neurones in area 17 of the cat.Experimental Brain Research38,431–435.CrossRefGoogle ScholarPubMed
Toyama,K.,Kimura,M. &Tanaka,T. (1981).Organization of cat visual cortex as investigated by cross-correlation technique.Journal of Neurophysiology46,202–214.CrossRefGoogle ScholarPubMed
Ullman,S. &Schechtman,G. (1982).Adaptation and gain normalization.Proceedings of the Royal Society B (London)216,299–313.Google ScholarPubMed
Vautin,R.G. &Berkeley,M.A. (1977).Responses of single cells in cat visual cortex to prolonged stimulus movement: Neural correlates of visual aftereffect.Journal of Neurophysiology40,1051–1065.CrossRefGoogle Scholar
Vidyasaoar,T.R. (1990).Pattern adaptation in cat visual cortex is a cooperative phenomenon.Neuroscience36,175–179.CrossRefGoogle Scholar
von der Heydt,R.,Hanny,P. &Adorjani,C. (1978).Movement aftereffects in the visual system.Archives of Italian Biology116,248–254.Google Scholar